Footprints of natural selection at the mannose-6-phosphate isomerase locus in barnacles
Open Access
- 25 February 2020
- journal article
- research article
- Published by Proceedings of the National Academy of Sciences in Proceedings of the National Academy of Sciences of the United States of America
- Vol. 117 (10), 5376-5385
- https://doi.org/10.1073/pnas.1918232117
Abstract
The mannose-6-phosphate isomerase (Mpi) locus in Semibalanus balanoides has been studied as a candidate gene for balancing selection for more than two decades. Previous work has shown that Mpi allozyme genotypes (fast and slow) have different frequencies across Atlantic intertidal zones due to selection on postsettlement survival (i.e., allele zonation). We present the complete gene sequence of the Mpi locus and quantify nucleotide polymorphism in S. balanoides, as well as divergence to its sister taxon Semibalanus cariosus. We show that the slow allozyme contains a derived charge-altering amino acid polymorphism, and both allozyme classes correspond to two haplogroups with multiple internal haplotypes. The locus shows several footprints of balancing selection around the fast/slow site: an enrichment of positive Tajima’s D for nonsynonymous mutations, an excess of polymorphism, and a spike in the levels of silent polymorphism relative to silent divergence, as well as a site frequency spectrum enriched for midfrequency mutations. We observe other departures from neutrality across the locus in both coding and noncoding regions. These include a nonsynonymous trans-species polymorphism and a recent mutation under selection within the fast haplogroup. The latter suggests ongoing allelic replacement of functionally relevant amino acid variants. Moreover, predicted models of Mpi protein structure provide insight into the functional significance of the putatively selected amino acid polymorphisms. While footprints of selection are widespread across the range of S. balanoides, our data show that intertidal zonation patterns are variable across both spatial and temporal scales. These data provide further evidence for heterogeneous selection on Mpi.Keywords
Funding Information
- National Science Foundation (DGE-0966060)
- HHS | NIH | National Institute of General Medical Sciences (2R01GM067862)
- Carl Tryggers Stiftelse för Vetenskaplig Forskning (CTS 11:14)
- Svenska Forskningsrådet Formas (2017-04559)
- Svenska Forskningsrådet Formas (2014-03914)
- National Science Foundation (GRFP)
- National Science Foundation (GROW)
- NSF | OD | OIA | Office of Experimental Program to Stimulate Competitive Research (Fellowship)
- Brown University (UTRA)
This publication has 69 references indexed in Scilit:
- LDx: Estimation of Linkage Disequilibrium from High-Throughput Pooled Resequencing DataPLOS ONE, 2012
- Adaptation of Drosophila to a novel laboratory environment reveals temporally heterogeneous trajectories of selected allelesMolecular Ecology, 2012
- Genetic Structure and the North American Postglacial Expansion of the Barnacle, Semibalanus balanoidesJournal of Heredity, 2011
- MSMS: a coalescent simulation program including recombination, demographic structure and selection at a single locusBioinformatics, 2010
- Statistical Power Analysis of Neutrality Tests Under Demographic Expansions, Contractions and Bottlenecks With RecombinationGenetics, 2008
- A Map of Recent Positive Selection in the Human GenomePLoS Biology, 2006
- From DNA to Fitness Differences: Sequences and Structures of Adaptive Variants of Colias Phosphoglucose Isomerase (PGI)Molecular Biology and Evolution, 2005
- Missense meanderings in sequence space: a biophysical view of protein evolutionNature Reviews Genetics, 2005
- Detecting recent positive selection in the human genome from haplotype structureNature, 2002
- Contrasting amounts of geographical variation as evidence for direct selection: the Mpi and Pgm loci in eight crustacean speciesHeredity, 1991